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Revista Colombiana de Ciencias Pecuarias
ISSN: 0120-0690
[email protected]
Universidad de Antioquia
Colombia
Olea, Gabriela B; Sandoval, María T
Embryonic development of Columba livia (Aves: Columbiformes) from an altricial-precocial perspective
Revista Colombiana de Ciencias Pecuarias, vol. 25, núm. 1, enero-marzo, 2012, pp. 3-13
Universidad de Antioquia
Medellín, Colombia
Available in: http://www.redalyc.org/articulo.oa?id=295023572002
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Olea GB et al. Embryonic development of Columba livia
3
Artículos originales
Revista Colombiana de Ciencias Pecuarias
Embryonic development of Columba livia (Aves:
Columbiformes) from an altricial-precocial perspective¤
Desarrollo embrionario de Columba livia (Aves: Columbiformes) desde una perspectiva altricial-precoz
Desenvolvimento embrionário de Columba livia (Aves: Columbiformes) a partir de uma perspectiva
altricial-precoce
Gabriela B Olea1, Lic Cienc Biol; María T Sandoval1*, Lic Cienc Biol.
1
Laboratorio de Herpetología. Departamento de Biología. Facultad de Ciencias Exactas y Naturales y Agrimensura –
Universidad Nacional del Nordeste.
Avenida Libertad, 5470 (3400) Corrientes, Argentina.
(Recibido: 28 enero, 2011; aceptado: 29 septiembre, 2011)
Summary
Objective: this study characterized the morphogenesis of Columba livia and proposed a table with
43 embryonic stages. The ontogeny of this species was divided into three phases: early, middle and late.
Methods and Results: the early phase (stages 1-26) includes the final period of segmentation, gastrulation,
neurulation and somitogenesis, organization of the extraembryonic membranes, and the initial formation
of the major organic systems. The middle phase (stages 27-36) was characterized mainly by the growth of
limbs and the organization of the autopodium, the formation and growth of the peak, and the development
of integumentary annexes such as feather germs and leg scales. The late phase (stages 37-43) shows the
overall embryo growth, the final organization of the pterilosis pattern and growth of feather germs, as well
as final consumption of the yolk, and hatching. Conclusions: these results allow making comparisons with
the proposed developmental events of Gallus gallus domesticus, highlighting similarities and differences
in the ontogenetic sequence of both species. Therefore we propose some hypotheses about possible
heterochronic events related to altricial-precocial developmental models.
Key words: Columbidae, development patterns, embryonic stages, ontogeny.
Resumen
Objetivo: en el presente trabajo se caracteriza la morfogénesis de Columba livia y se propone una tabla
con 43 estadios embrionarios. La ontogenia de dicha especie fue dividida en tres etapas: temprana, media y
tardía. Métodos y Resultados: la etapa temprana (estadios 1-26) incluye el periodo final de la segmentación,
¤ To cite this article: Olea GB, Sandoval MT. Embryonic development of Columba livia (Aves: Columbiformes) from an altricial-precocial perspective. Rev
Colomb Cienc Pecu 2012; 25:3-13.
* Corresponding author: María T Sandoval. Avenida Libertad, 5470 (3400) Corrientes, Argentina. E-mail: [email protected]
Rev Colomb Cienc Pecu 2012; 25:3- 13
4
Olea GB et al. Embryonic development of Columba livia
la gastrulación, neurulación y somitogénesis, la organización de las membranas extraembrionarias y
la formación de los esbozos de los principales sistemas de órganos. La etapa media (estadios 27-36) se
caracteriza principalmente por el crecimiento de los miembros y la organización del autopodio, la formación
y crecimiento del pico y el desarrollo de los anexos tegumentarios como plumones y escamas de las patas.
En la etapa tardía (estadios 37-43) se evidencia el crecimiento general del embrión, la organización final
del patrón de pterilosis y crecimiento de plumones, como así también el consumo final del vitelo y la
eclosión. Conclusiones: en base a los resultados obtenidos se realizan algunas comparaciones con respecto
a los eventos del desarrollo propuestos para Gallus gallus domesticus, destacando semejanzas y diferencias
en la secuencia ontogénetica de ambas especies. A partir de esto se plantean algunas hipótesis acerca de
posibles eventos heterocrónicos relacionados con los modelos de desarrollo altricial-precoz.
Palabras clave: Columbidae, estados de desarrollo embrionario, ontogenia.
Resumo
Objetivo: no presente trabalho caracteriza-se a morfogênese de Columba livia, mediante uma tabela
com 43 estágios embrionários. A ontogenia desta espécie foi dividida em três etapas: inicial, intermediária
e final. Métodos y Resultados: a etapa inicial (estágios 1-26) incluiu o período final de segmentação,
gastrulação, neurulação e somitogênese, organização das membranas extraembrionárias e formação
dos esboços dos principais sistemas de órgãos. A etapa intermediária (estágios 27-36) foi caracterizada
principalmente pelo crescimento dos membros e organização do autopódio, formação e crescimento do
bico e desenvolvimento de anexos tegumentários como as penas e as escamas das patas. Na etapa tardia
(estágios 37-43) foi caracterizada pelo crescimento geral do embrião, a organização final do padrão de
pterilose e o padrão de crescimento das penas, assim como o consumo final do vitelo e eclosão. Conclusões:
com base nos resultados obtidos, foram realizadas algumas comparações com respeito aos eventos do
desenvolvimento proposto para Gallus gallus domesticus, destacando semelhanças e diferenças durante
a sequência ontogenética de ambas espécies. A partir disso, algumas hipóteses são propostas acerca dos
possíveis eventos heterocrônicos relacionados com os modelos de desenvolvimento altricial e precoce.
Palavras chave: Columbidae, estádios de desenvolvimento embrionário, ontogenia, padrões de
desenvolvimento.
Introduction
The embryology of vertebrates has been
extensively studied in model organisms such as
Danio rerio (Kimmel et al., 1995), Xenopus laevis
(Keller, 1991), Bufo arenarum (Del Conte and
Sirlin, 1951; Echeverria and De López, 1981), and
Rattus norvegicus (Tam and Beddington, 1987)
for which there is extensive information regarding
the ontogenetic sequence and the morphology of
different stages. In the case of birds, most of the
knowledge on embryonic morphology has been
derived from studies of Gallus gallus domesticus.
Based on embryonic morphological characteristics,
Hamburger and Hamilton (1952) established a table
with 46 stages of development, which is used as a
benchmark for many studies that have birds as the
experimental model (Bellairs, 1958; Chevallier,
1977; Brush et al., 1972; Couly et al., 1992;
Caprioli et al., 1998).
Other studies on bird development have
addressed precocial bird species such as Colinus
virginianus (Hendrickx and Hanzlik, 1965), Anas
boschas domestica (Koecke 1958), Meleagris
gallopavo (Mun and Kosin, 1960), Coturnix
coturnix japonica (Ainsworth et al., 2009), and
altricial species such as Lonchura striata (Yamasaki
and Tonosaki, 1988) and Tyto alba (Köppl et al.,
2005), although only partial information on their
embryonic ontogeny is currently available. These
reports indicate existing developmental variations
in certain structures between species, which are
related to the status of the chicks at hatching or,
according to Yamasaki and Tonosaki (1988), are
in¯uenced by altricial or precocial developmental
Rev Colomb Cienc Pecu 2012; 25:3-13
Olea GB et al. Embryonic development of Columba livia
models. There are marked differences between
early and altricial species speci®cally during the
period when ontogenetic events occur. Starck &
Ricklefs (1998) state that precocial species have
higher rates of embryonic development so that
at the time of hatching their organs are in a more
advanced state of functional maturity as compared
with altricial species. These differences demonstrate
that the correspondence or assignment of a bird’s
embryonic stage based on a single reference table
as established by Hamburger and Hamilton (1952)
would not be valid for all taxa.
Columba livia is a cosmopolitan and ¯ying
species with urban and suburban habits and a type2 semialtricial development model (Starck and
Ricklef, 1998). Given the ease of egg collection,
laboratory incubation, and biological peculiarities,
this species is a good model for embryological
studies and has been used in many studies on the
development of organ systems (Chevallier, 1977;
Teillet, 1978; Caprioli et al., 1998, Pardanaud and
Dieterlen-Lièvre, 1999). Currently, this species
is used in genetic and developmental biology
studies (Kuroda et al., 1990; Schultheiss et al.,
1995; Petitte et al., 2004; Petitte, 2006), which
require the identi®cation of embryonic stages.
However, there is no information on the ontogeny
of Columba livia so the assignment of embryonic
stage allocations is based on the Gallus gallus
domesticus table. In this paper we address the study
of the developmental sequence of Columba livia
with the aim of producing a table of embryonic
stages based on external morphological characters
that would facilitate its identi®cation. Additionally,
the differences and/or similarities in the embryonic
sequence of this species with the sequence proposed
for Gallus gallus domesticus were analyzed in order
to provide data that will allow the identi®cation of
patterns related to altricial and precocial models.
Materials and methods
Materials
Fertile eggs from Columba livia were collected
on the Facultad de Ciencias Exactas y Naturales y
Agrimensura campus of the Universidad Nacional del
Rev Colomb Cienc Pecu 2012; 25:3- 13
5
Nordeste (Corrientes, Argentina) during the nesting
period. At this location the animals build their nests
in holes and depressions on the roof and lay 2 eggs on
alternating days. For the present study 10 nests were
randomly selected to be checked daily or weekly for
fertilized eggs from September to March 2008-2009
and 2009-2010. The eggs were collected early in
the morning to ensure they were recently laid. Eggs
were arti®cially incubated in a culture stove at 35-37
°C with approximately 40-45% humidity to obtain
embryos in different stages of development. Fixation
of the embryos in 10% formalin was performed
according to the following protocol: every 1-4 hours
during the ®rst 5 days, then every 6-10 hours, until the
tenth day and then every 12-24 hours, to complete the
development. To slaughter the specimens, the standard
method established in the Guidelines for Animal
Euthanasia proposed by the IACUC (Institutional
Animal Care and Use Committee) was followed. A
stereoscopic microscope was used to separate yolks
from embryos, which were cleaned and subsequently
stained with methylene blue. The analyzed material
became part of the scienti®c collection of the
animal embryology course of the Department of
Biology, Facultad de Ciencias Exactas y Naturales
y Agrimensura of the Universidad Nacional del
Nordeste.
Embryo analysis
A total of 190 embryos in various stages of
development were analyzed: 100 in early phase
(stages 1-26), 55 in middle phase (stages 27-36)
and 35 in late phase (stages 37-43). Each stage was
characterized based on the external morphological
traits considered by Hamburger and Hamilton
(1952) in addition to other traits not considered by
these authors (see text). Stage 2 was divided into
sub-stages a, b, and c, considering they represent the
same process (formation of the primitive streak) in
different periods.
The following were measured during stages
3-12: the length of the zona pellucida (LZP),
the length of the primitive streak (LLP), and the
total length (Lt) of the embryo pondered from the
anterior end of the plate/neural tube to the posterior
end of the primitive streak.
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Olea GB et al. Embryonic development of Columba livia
During stages 28-43 the length of the maxillary
process (Lpmx) and length of mandibular process
(Lpm) were measured. These measurements were
made with an ocular micrometer incorporated in
the stereomicroscope. For stages 37-42 a graduated
cylinder was used to measure the embryo volume
(Ve) and yolk volume (Vv). Using these data, total
volume (Vt) was calculated as Vt = Ve + Vv. The
morphology of lungs was described based upon
the method proposed by Chuong et al. (2000).
Photographs of the embryos were taken with a
Canon A2000 IS digital camera.
Results
Early phase (Figure 1)
Stage 1 (± 3 h of incubation): zona pellucida and
Zona opaca circularly shaped. Blastoderm in the
central portion of the zona pellucida.
Stage 2a (± 8 h of incubation): zona pellucida
inverted pear-shape. Primitive streak visible in the
rear end of the zona pellucida. Llp LZP ± 25%.
Stage 2b (± 10 h incubation): zona pellucida
inverted pear-shape. Llp LZP ± 50%.
Stage 2c (± 12 h incubation): zona pellucida
inverted pear-shape. Llp LZP ± 70%. Primitive
streak groove, and Hensen’s node clearly
distinguishable.
Stage 3 (± 14 h incubation): primitive streak
similar to previous stage. Neural plate visible in
front of the primitive streak.
Stage 4 (± 17 h of incubation): neural folds and
neural groove visible in the anterior neural plate.
Llp ± 75% of the Lt of the embryo. Blood islands
are visible in the posterior region of the opaque
area.
Stage 5 (± 18 h incubation): two pairs of
somites. Deeper neural groove. Neural folds close
together in the dorsal midline of the anterior region.
Llp ± 65% of the Lt of the embryo. Blood islands as
previously described.
Stage 6 (± 20 h incubation): three pairs of
somites. Neural folds similar to the previous stage.
Llp ± 50% of the Lt of the embryo. Patterns of
vitelline vessels visible in the posterior region of the
vitelline membrane.
Stage 7 (± 21 h incubation): four pairs of
somites. Neural folds fused at the medial and
posterior brain. Anterior region open. Llp ± 45% of
the Lt of the embryo. Vitelline vessels extend to the
middle region of the membrane sac.
Stage 8 (± 23 h incubation): ®ve pairs of
somites. Three delimited brain vesicles (forebrain,
midbrain and hindbrain). Anterior neuropore is
open. Neural folds of trunk unfused. Llp ± 37% of
the Lt of the embryo. Vitelline vessels extending to
the anterior region of the vitelline membrane.
Stage 9 (± 26 h incubation): six-seven pairs of
somites. Forebrain expanded laterally to form optic
vesicles. Anterior neuropore open. Neural folds of
trunk and Llp as described above. Two endocardial
tubes visible in the ventrally pharyngeal region
of the embryo. Vitelline vessels extending to the
anterior region of the vitelline membrane.
Stage 10 (± 27 h incubation): 9 pairs of somites.
Forebrain with laterally expanded optic vesicles,
well delineated midbrain and hindbrain. Anterior
neuropore is closing. Neural folds of trunk fused at
the level of the somites, unfused into the posterior
region. Llp ± 20% of the Lt of the embryo.
Endocardial tubes fused in the midline with vitelline
veins projected laterally from the posterior region.
Well-de®ned vitelline vessels in the vitelline
membrane.
Stage 11 (± 28 h incubation): 11 pairs of
somites. Telencephalon curved toward the anterior
ventral region. Optic placodes distinguishable as
thickenings on both sides of the optic vesicles.
Neural folds of trunk unfused in the posterior
region. Llp ± 20% of the Lt of the embryo. In
ventral view, a tubular heart with a posterior
widening corresponding to the venous sinus. Idem
vitelline vessels.
Rev Colomb Cienc Pecu 2012; 25:3-13
Olea GB et al. Embryonic development of Columba livia
Stage 12 (± 29 h incubation): 13 pairs of somites.
More developed telencephalon and optic vesicles
visible ventrally. More prominent midbrain, with six
rombomeres in the hindbrain (r1-r6). Otic placodes in
process of invagination visible dorsally at r5-r6. Llp ±
15% of the LT. S-shaped curved heart. Vitelline veins
connected to the vessels of the vitelline membrane.
Evident heartbeat. Amniotic membrane visible
in the anterior region of the embryo covering the
procencephalon and midbrain. Vitelline membrane
covering approximately 1/4 of the yolk mass.
Stage 13 (± 32 h incubation): 16 pairs of
somites. Cephalic region curved to the right.
Telencephalon and mesencephalon more prominent.
Mesencephalic ¯exure distinguishable. r2 r1
more dilated than others. Invaginated lens vesicle,
optic cup with distinguishable choroidal ®ssure.
Invaginated otic vesicle visible at the level of r5r6. Llp ± 7% of the Lt of the embryo. Heart with
4 chambers well de®ned, expanded laterally to
the right. Anterior fold of the amnion extends to
the posterior region of the hindbrain. Vitelline
membrane similar to the previous stage.
Stage 14 (± 36-40 h incubation): 19-22 pairs
of somites. Curvature of the embryo to the right
extends to the ®rst somite. Eye and otic vesicle
similar to previous stage. First and Second visceral
arches present. Primitive streak absent. Welldeveloped vitelline vascular system. Well-developed
vitelline arteries and visible at the level of somite
15-16. Atrial and ventricular more prominent than
other cardiac chamber, no obvious septa. Anterior
fold of the amnion extends to the level of somite 7.
Stage 15 (± 40-44 h incubation): 25 pairs of
somites. Curvature of the embryo to the right
more pronounced. Midbrain more prominent
than the other brain vesicles. Cervical ¯exion
distinguishable. Eye more prominent with the onset
of retinal pigmentation. Auditory vesicle shows
dorsal endolymphatic duct. First, second, third, and
fourth visceral arches present, the second being the
largest. Nasal placodes in lateroventral position
visible in the anterior region of the head. Anterior
fold of the amnion covers the embryo to the level of
somite 14. Vitelline membrane covering about 1/3
of the yolk mass.
Rev Colomb Cienc Pecu 2012; 25:3- 13
7
Stage 16 (± 44-46 h incubation): 26-28 pairs of
somites. Invaginated nasal placode. Anterior amnion
fold covers the embryo until the 17 somite; lateral
amnion folds visible in the posterior region of the
embryo. Distinctive anterior limb bud at the height
of 12-14 somites as a lateral expansion. Other
structures similar to the previous stage.
Stage 17 (± 48-54 h incubation): 30 to 36 pairs
of somites. More pronounced curvature of the
embryo. Telencephalon divided into two distinct
vesicles visible laterally. Epiphysis visible in the
dorsal region of the diencephalon. Midbrain divided
into bulky lobes. Four visceral arches present;
the second is largest and the fourth is very small.
Posterior limb bud visible at the level of somite
25-30. Caudal end is ventrally curved. Anterior
fold of the amnion extends to the posterior region
of the embryo, lateral folds fused with anterior
and posterior, except in the posterior dorsal region.
Allantois visible as a small ventral saccular
evagination between the posterior limb buds.
Stage 18 (± 54-63 h incubation): 37-40 pairs
of somites. Embryo is C-shaped with large head.
Midbrain well developed. Eye prominent with a
more pigmented retina. Visceral arch 1 divided
into maxillary and mandibular processes, third
and fourth visceral arches not visible. Anterior
and posterior limb buds equal length. Amnion
completely formed. Allantois more prominent than
previous stage and laterally visible in the posterior
region of the embryo. Vitelline membrane covering
about half of the yolk mass with well-developed
arterial and venous vessels.
Stage 19 (± 63-69 h incubation): 40-43 pairs
of somites. Maxillary process longer than the
mandibular process. Second visceral arch visible.
Limb buds are as long as wide. Allantois more
developed than previous stage with patterns of
blood vessels.
Stage 20 (± 69-96 h incubation): 44 pairs of
somites. Curvature of the embryo more pronounced.
Mandibular process extends to the middle of
the maxillary process. Second visceral arch
inconspicuous. Heart with ventricle prominently
located posteroventral to the right and left atria.
8
Olea GB et al. Embryonic development of Columba livia
Limb buds more developed. Allantois larger and
well vascularized.
Stage 21 (4 days of incubation): the embryo
becomes white, internal structures not clearly
visible. Optic lobes very prominent. Eyes are large.
Second visceral arch visible as a ventrolateral
expansion posterior to the mandibular process.
Limb bud oar-shaped. Allantois completely covers
the embryo. Embryo produces muscular torsional
movements.
Stage 22 (5 days of incubation): anterior end
of the maxillary process close to the nostrils.
Anterior end of the mandibular process joint in the
midline. Stomodeum plate closed. Limb buds more
developed. Allantois larger than previous stage.
Smooth integument.
Stage 23 (5 ½ days of incubation): maxillary
process exceeds previously to the nostrils.
Mandibular process reaches half the length of the
maxillary process. Stomodeum plate perforated.
Differentiated second visceral arch not visible.
Longer limbs with distinguishable digital plates in
the autopod region. Vitelline membrane completely
covers the yolk mass.
Stage 24 (6 days of incubation): auditive duct
visible behind the mandibular process. Large
eyes. Articulation member between stylopod and
zeugopod. Forelimb autopod with notch between
digits 1 and 2.
Stage 25 (6 ½ days of incubation): limbs longer
in length. Autopod of the forelimb and posterior
recesses between digits 1 and 2 and 2 and 3.
Stage 26 (7 days of incubation): maxillary
process longer and curved down. Forelimb
interdigital notches sharper. Interdigital notch
between ®nger 3 and 4 of the hind limb visible.
Longer neck.
Figure 1: Embryonic stages (E) of early development of Columba livia. Scale: 0.05 mm. (E. 1-17), 1 mm. (E.18-26).
Rev Colomb Cienc Pecu 2012; 25:3-13
Olea GB et al. Embryonic development of Columba livia
Middle phase (Figure 2)
Stage 27 (7 ½ days of incubation): maxillary
process with egg-tooth on the dorsal side.
Mandibular process extended to half the length of
the maxillary process. Hind limb with digits 2, 3,
and 4 dorsally visible; digit 1 in a ventral position.
Primordial feather germ placode-shaped distributed
in two dorsal rows and two caudal rows.
Stage 28 (8 days of incubation): mandibular and
maxillar process form distinguishable beak. Beak:
Lpmx: 5.49 mm and Lpm: 4.27 mm. Digit 2 of the
forelimb longer than the others. Webbing of the hind
limb transparent. Primordial feather germ placode
shaped distributed in 4 dorsal rows and 3 caudal
rows. 4 scleral papillae visible on the eyeball.
Stage 29 (8 ½ days of incubation): beak:
Lpmx: 5.73 mm and Lpm: 4.51 mm. Limbs more
developed than in the previous stage. Digit 3 of the
hind limb longer than others. Primordial feather
germ placode shaped distributed in 4 spinal rows,
5-6 lumbo-sacral rows, 2 femoral rows, 2 scapular
rows. Primordial feather germ reticulum-shaped
distributed in 4 cuadal rows. 6-7 scleral papillae
arranged in a semicircle on the eyeball. Eyelid rim
visible around the eyeball.
Stage 30 (9 days of incubation): beak: Lpmx:
5.98 mm and Lpm: 4.76 mm. Forelimb wing-like.
Webbing of the limb buds absent. Primordial feather
germ placode shaped distributed in 2 marginal
spinal rows, 7 lumbo-sacral rows, 4 femoral rows,
4 scapular rows, 1 row around the duct auditive,
and dispersed pectoral and capital primordial.
Primordial feather germ reticulum shaped
distributed in the 2 medial rows and 4 spinal caudal
rows.13 scleral papillae around the eyeball.
Stage 31 (9 ½ days of incubation): beak: Lpmx:
6.1 mm and Lpm: 4.88 mm. Limbs developed.
Rev Colomb Cienc Pecu 2012; 25:3- 13
9
Eyelid covers half of the eyeball. Primordial feather
germ reticulum shaped distributed throughout the
body except the ventral region of the neck and
abdomen.
Stage 32 (10 days of incubation): beak: Lpmx:
6.1 mm and Lpm: 5.49 mm. Phalanges of the hind
limb distinguishable. Primordial feather germ
reticulum shaped in the ventral region of the neck
and entire body except in the abdominal region.
Upper and lower eyelids cover the eye scleral
papillae. Nictitating membrane visible in the vertice
of the eye. Chorioallantoideal membrane closely
attached to the eggshell.
Stage 33 (10 ½ days of incubation): beak: Lpmx:
6.8 mm and Lpm: 6.34 mm. Primordial feather
germ conical-shaped in the dorsal part of the body;
the rest form a lattice. Filiform feather germ in the
wing and femoral tract. Footpads and claws not yet
corni®ed.
Stage 34 (11 days of incubation): beak: Lpmx:
7.93 mm and Lpm: 9.37 mm with prominent egg
tooth. Contour eyeling oval-shaped. Patterns of
scales slightly visible on the front of the hind limb.
Footpads well differentiated onset corni®cation in
claws. Feathers similar to the previous stage.
Stage 35 (11 ½ days of incubation): beak: Lpmx:
8.54 mm and Lpm: 10.98 mm. Filiform markers
throughout the body except in the circumorbital
region and around the auditive duct where they
remain reticulum-shaped. Leg scales arranged in
imbricate form.
Stage 36 (12 days of incubation): beak: Lpmx:
10.04 mm and Lpm: 11.83 mm. Long thread-like
feathers in trunk region, short feathers on the head
region, neck, and wing. Footpads with pattern of
scales visible as papillae. Claws well corni®ed.
Eyelid covers most of the eye.
10
Olea GB et al. Embryonic development of Columba livia
Figure 2: Stages of mid-stage embryonic development of Columba livia. Scale: 2 mm.
Stage 37 (12 ½ days of incubation): Vv = 5040% / Vt. Beak: Lpmx: 10.37 mm and Lpm: 12.2
mm. Feathers similar to the previous stage, but
corneal sheath.
Stage 41 (15 days of incubation): Vv = <10%
/ Vt. Beak: Lpmx: 12.2mm and Lpm: 15.25mm.
Feathers have lost the sheath cornea. Eyelids same
as previous stage.
Stage 38 (13 days of incubation): Vv = 40-25%
/ Vt. Beak: Lpmx: 10.49 and Lpm: 12.4 mm, well
corni®ed. Filiform feathers longer than previous
stage. Footpads covered with granular scales.
Eyelids cover the lenses.
Stage 42 (16 days of incubation): Yolk
completely incorporated into the abdominal cavity
of the embryo. Feathers acquired yellow color.
Beak: Lpm Lpmx idem to previous stage. Eyelid
same as previous stage. Onset of egg shells breaking
(time ± 24 h).
Stage 39 (13 ½ days of incubation): Vv = 2520% / Vt. Beak: Lpm Lpmx idem to previous stage.
Feathers are longer.
Stage 43 (± 17 days): Neonate with closed
eyelids and low mobility.
Stage 40 (14 days of incubation): Vv = 20-10%
/ Vt. Closed eyelids, not fused. All others similar to
the previous stage.
Rev Colomb Cienc Pecu 2012; 25:3-13
Olea GB et al. Embryonic development of Columba livia
11
Figure 3: Late-stage embryonic development stages of Columba livia. Scale: 5 mm.
Discussion
Hendrickx and Hanzlik (1965) described the
ontogeny of Colinus virginianus pointing at a
gradual delay in the development of this species
compared to what was described by Hamburger
and Hamilton (1952). Yamasaki and Tonosaki
(1988) found differences between Lonchura striata
var domestica and Gallus gallus domesticus in
the following: the development and duration of
the primitive streak, neural folds, brain, retinal
pigmentation, and feathers. Köppl et al. (2005)
reported the normal developmental sequence of
Tyto alba and exposed differences found with
respect to the ontogeny of the chicken concerning
the development of the eyelids and feather germs.
Likewise, Ainswort et al. (2009) compared the
morphogenesis and feather germ pigmentation, the
development of the beak and toes between Coturnix
coturnix japonica and Gallus gallus domesticus,
Rev Colomb Cienc Pecu 2012; 25:3- 13
and identi®ed variations in the developmental time,
mainly during late ontogenetic stages.
Regard ing the observations of the present study,
Columba livia domesticus showed similarities
with Gallus gallus domesticus in the ontogenetic
sequence of events during the early stages of
development. These include the formation of the
primitive streak, the appearance of the neural
plate and consequent formation of the neural folds
and neural tube, the formation of the primary
circulatory system, and the organization of extraembryonic membranes. However, consistent
with what has been reported by other authors, we
observed differences in middle and late stages
corresponding mainly to the timing of appearance of
limb buds, the growth of the beak, the development
of feathers and the organization and corni®cation
of legs, scales, and claws. Considering the
stages and developmental time, these structures
appear earlier in Columba livia than in Gallus
12
Olea GB et al. Embryonic development of Columba livia
gallus domesticus. These differences could be
explained by the morphological characteristics
of neonates and the incubation of eggs, which
are 17 and 21 days, respectively. Upon hatching,
the chicks of these species differ in the degree of
functional maturity of some organ systems, such
as muscular, and in behavioral aspects, such as
nest permanence and feeding by parents, which
are characteristics associated with semialtricial-2
and precocial-2 developmental models (Starck
and Ricklefs, 1998; Pough et al., 2003). However,
the external morphology of hatchlings is similar
in the development of feathers, scales, claws,
beak, and eyes. In this regard, we believe that the
advancement in time of these characteristically
morphogenetic events allows Columba livia to reach
a degree of morphological development similar
to that of Gallus gallus domesticus in a shorter
time period and represents a clear example of
heterochrony in the ontogeny of these species.
Blom and Lilja (2005) described differences in
developmental time and maturation of the digestive
system, muscular somite formation and size of
the brain, eyes, and locomotive organs among
precocial and altricial species with different patterns
of postnatal growth. In conclusion, they suggest
that the assessment of embryonic growth rate is
essential to characterize the patterns of development
and also offers an excellent opportunity to analyze
heterochonyc events. Based on the results of the
present study we propose that the analysis and
comparison of ontogenetic sequences of varying
species of birds with different developmental
models is also important not only to obtain a wider
knowledge of embryonic characteristics in each
species, but also to identify ontogenetic patterns
related to altricial and precocial models.
Acknowledgements
To Lic. Alejandra Hernando and Lic. Blanca
Beatriz Alvarez de Avanza for their critical reading
of the manuscript and their comments as well as the
General Secretariat of Science and Technology of
the Universidad Nacional del Nordeste for funding
this work (Res. 740/07 CS). We also thank the
suggestions and corrections made by this paper’s
reviewers as they substantially contributed to
improve the quality of the manuscript.
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